Stewardship of global collective behavior.

Collective behavior provides a framework for understanding how the actions and properties of groups emerge from the way individuals generate and share information. In humans, information flows were initially shaped by natural selection yet are increasingly structured by emerging communication technologies. Our larger, more complex social networks now transfer high-fidelity information over vast distances at low cost. The digital age and the rise of social media have accelerated changes to our social systems, with poorly understood functional consequences. This gap in our knowledge represents a principal challenge to scientific progress, democracy, and actions to address global crises. We argue that the study of collective behavior must rise to a "crisis discipline" just as medicine, conservation, and climate science have, with a focus on providing actionable insight to policymakers and regulators for the stewardship of social systems.

Long-distance vocalizations of spotted hyenas contain individual, but not group, signatures.

In animal societies, identity signals are common, mediate interactions within groups, and allow individuals to discriminate group-mates from out-group competitors. However, individual recognition becomes increasingly challenging as group size increases and as signals must be transmitted over greater distances. Group vocal signatures may evolve when successful in-group/out-group distinctions are at the crux of fitness-relevant decisions, but group signatures alone are insufficient when differentiated within-group relationships are important for decision-making. Spotted hyenas are social carnivores that live in stable clans of less than 125 individuals composed of multiple unrelated matrilines. Clan members cooperate to defend resources and communal territories from neighbouring clans and other mega carnivores; this collective defence is mediated by long-range (up to 5 km range) recruitment vocalizations, called whoops. Here, we use machine learning to determine that spotted hyena whoops contain individual but not group signatures, and that fundamental frequency features which propagate well are critical for individual discrimination. For effective clan-level cooperation, hyenas face the cognitive challenge of remembering and recognizing individual voices at long range. We show that serial redundancy in whoop bouts increases individual classification accuracy and thus extended call bouts used by hyenas probably evolved to overcome the challenges of communicating individual identity at long distance.

Accelerometer-based predictions of behaviour elucidate factors affecting the daily activity patterns of spotted hyenas.

Animal activity patterns are highly variable and influenced by internal and external factors, including social processes. Quantifying activity patterns in natural settings can be challenging, as it is difficult to monitor animals over long time periods. Here, we developed and validated a machine-learning-based classifier to identify behavioural states from accelerometer data of wild spotted hyenas (Crocuta crocuta), social carnivores that live in large fission-fusion societies. By combining this classifier with continuous collar-based accelerometer data from five hyenas, we generated a complete record of activity patterns over more than one month. We used these continuous behavioural sequences to investigate how past activity, individual idiosyncrasies, and social synchronization influence hyena activity patterns. We found that hyenas exhibit characteristic crepuscular-nocturnal daily activity patterns. Time spent active was independent of activity level on previous days, suggesting that hyenas do not show activity compensation. We also found limited evidence for an effect of individual identity on activity, and showed that pairs of hyenas who synchronized their activity patterns must have spent more time together. This study sheds light on the patterns and drivers of activity in spotted hyena societies, and also provides a useful tool for quantifying behavioural sequences from accelerometer data.

Zebras of all stripes repel biting flies at close range.

The best-supported hypothesis for why zebras have stripes is that stripes repel biting flies. While this effect is well-established, the mechanism behind it remains elusive. Myriad hypotheses have been suggested, but few experiments have helped narrow the field of possible explanations. In addition, the complex visual features of real zebra pelage and the natural range of stripe widths have been largely left out of experimental designs. In paired-choice field experiments in a Kenyan savannah, we found that hungry Stomoxys flies released in an enclosure strongly preferred to land on uniform tan impala pelts over striped zebra pelts but exhibited no preference between the pelts of the zebra species with the widest stripes and the narrowest stripes. Our findings confirm that zebra stripes repel biting flies under naturalistic conditions and do so at close range (suggesting that several of the mechanisms hypothesized to operate at a distance are unnecessary for the fly-repulsion effect) but indicate that interspecific variation in stripe width is associated with selection pressures other than biting flies.

Physiology modulates social flexibility and collective behaviour in equids and other large ungulates.

Though morphologically very similar, equids across the extant species occupy ecological niches that are surprisingly non-overlapping. Occupancy of these distinct niches appears related to subtle physiological and behavioural adaptations which, in turn, correspond to significant differences in the social behaviours and emergent social systems characterizing the different species. Although instances of intraspecific behavioural variation in equids demonstrate that the same body plan can support a range of social structures, each of these morphologically similar species generally shows robust fidelity to its evolved social system. The pattern suggests a subtle relationship between physiological phenotypes and behavioural flexibility. While environmental conditions can vary widely within relatively short temporal or spatial scales, physiological changes and changes to the behaviours that regulate physiological processes, are constrained to longer cycles of adaptation. Physiology is then the limiting variable in the interaction between ecological variation and behavioural and socio-structural flexibility. Behavioural and socio-structural flexibility, in turn, will generate important feedbacks that will govern physiological function, thus creating a coupled web of interactions that can lead to changes in individual and collective behaviour. Longitudinal studies of equid and other large-bodied ungulate populations under environmental stress, such as those discussed here, may offer the best opportunities for researchers to examine, in real time, the interplay between individual behavioural plasticity, socio-structural flexibility, and the physiological and genetic changes that together produce adaptive change.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Long-distance communication facilitates cooperation among wild spotted hyaenas, Crocuta crocuta.

Calls that catalyse group defence, as in the mobbing of predators, appear to facilitate cooperation by recruiting receivers to act collectively. However, even when such signals reliably precede cooperative behaviour, the extent to which the calls function as recruitment signals is unclear. Calls might simply arouse listeners' attention, setting off a cascade of independent responses to the threat. By contrast, they might convey information, for example, about signaller identity and the nature of a threat that affects receivers' decisions to participate. We explored this distinction by investigating a possible long-distance recruitment call used by spotted hyaenas. These social carnivores live in fission-fusion clans and individuals disperse widely within their territories. Putative recruitment calls must therefore attract receivers that are distant from the inciting threat and free to opt out of risky collective aggression. Hyaenas compete with lions over food, and neighbouring clans sometimes engage in violent border clashes. These high-stakes contests are decided based on numerical asymmetries, so hyaenas can only protect critical resources if the dispersed clan can converge quickly at conflict sites. We recorded and analysed whoop bouts produced in multiple contexts and found that bouts produced in response to signs of lion-hyaena conflict had shorter inter-whoop intervals than spontaneous 'display' bouts. In subsequent field playback experiments, resting hyaenas were significantly more likely to move in response to 'recruitment' bouts with shortened intervals than to otherwise identical 'display' bouts. Whereas only stimulus type predicted movement, lower-ranked subjects responded most quickly, perhaps because their feeding opportunities depend on arriving early at any kill site. Results demonstrate that hyaenas possess a signal that can reliably recruit allies across long distances, despite moderating effects of individual circumstances on the strength of receivers' responses.

Social networks and the development of social skills in cowbirds.

The complex interrelationships among individuals within social environments can exert selection pressures on social skills: those behaviours and cognitive processes that allow animals to manipulate and out-reproduce others. Social complexity can also have a developmental effect on social skills by providing individuals with opportunities to hone their skills by dealing with the challenges posed in within-group interactions. We examined how social skills develop in captive, adult male brown-headed cowbirds (Molothrus ater) that were exposed to differing levels of 'social complexity' across a 2-year experiment. After each year, subjects housed in groups with dynamic social structure (where many individuals entered and exited the groups during the year) outcompeted birds who had been housed in static groups. Exposure to dynamic structure subsequently led to substantial changes to the social networks of the home conditions during the breeding season. Static groups were characterized by a predictable relationship between singing and reproductive success that was stable across years. In dynamic conditions, however, males showed significant variability in their dominance status, their courting and even in their mating success. Reproductive success of males varied dramatically across years and was responsive to social learning in adulthood, and socially dynamic environments 'trained' individuals to be better competitors, even at an age when the development of many traits important for breeding (like song quality) had ended.